Translocations: the genetic rescue paradox

14 01 2013

helphindranceHarvesting and habitat alteration reduce many populations to just a few individuals, and then often extinction. A widely recommended conservation action is to supplement those populations with new individuals translocated from other regions. However, crossing local and foreign genes can worsen the prospects of recovery.

We are all hybrids or combinations of other people, experiences and things. Let’s think of teams (e.g., engineers, athletes, mushroom collectors). In team work, isolation from other team members might limit the appearance of innovative ideas, but the arrival of new (conflictive) individuals might in fact destroy group dynamics altogether. Chromosomes work much like this – too little or too much genetic variability among parents can break down the fitness of their descendants. These pernicious effects are known as ‘inbreeding depression‘ when they result from reproduction among related individuals, and ‘outbreeding depression‘ when parents are too genetically distant.

CB_OutbreedingDepression Photo
Location of the two USA sites providing spawners of largemouth bass for the experiments by Goldberg et al. (3): the Kaskaskia River (Mississipi Basin, Illinois) and the Big Cedar Lake (Great Lakes Basin, Wisconsin). Next to the map is shown an array of three of the 72-litre aquaria in an indoor environment under constant ambient temperature (25 ◦C), humidity (60%), and photoperiod (alternate 12 hours of light and darkness). Photo courtesy of T. Goldberg.

Recent studies have revised outbreeding depression in a variety of plants, invertebrates and vertebrates (1, 2). An example is Tony Goldberg’s experiments on largemouth bass (Micropterus salmoides), a freshwater fish native to North America. Since the 1990s, the USA populations have been hit by disease from a Ranavirus. Goldberg et al. (3) sampled healthy individuals from two freshwater bodies: the Mississipi River and the Great Lakes, and created two genetic lineages by having both populations isolated and reproducing in experimental ponds. Then, they inoculated the Ranavirus in a group of parents from each freshwater basin (generation P), and in the first (G1) and second (G2) generations of hybrids crossed from both basins. After 3 weeks in experimental aquaria, the proportion of survivors declined to nearly 30% in G2, and exceeded 80% in G1 and P. Clearly, crossing of different genetic lineages increased the susceptibility of this species to a pathogen, and the impact was most deleterious in G2. This investigation indicates that translocation of foreign individuals into a self-reproducing population can not only import diseases, but also weaken its descendants’ resistance to future epidemics.

A mechanism causing outbreeding depression occurs when hybridisation alters a gene that is only functional in combination with other genes. Immune systems are often regulated by these complexes of co-adapted genes (‘supergenes’) and their disruption is a potential candidate for the outbreeding depression reported by Goldberg et al. (3). Along with accentuating susceptibility to disease, outbreeding depression in animals and plants can cause a variety of deleterious effects such as dwarfism, low fertility, or shortened life span. Dick Frankham (one of our collaborators) has quantified that the probability of outbreeding depression increases when mixing takes place between (i) different species, (ii) conspecifics adapted to different habitats, (iii) conspecifics with fixed chromosomal differences, and (iv) populations free of genetic flow with other populations for more than 500 years (2).

A striking example supporting (some of) those criteria is the pink salmon (Oncorhynchus gorbuscha) from Auke Creek near Juneau (Alaska). The adults migrate from the Pacific to their native river where they spawn two years after birth, with the particularity that there are two strict broodlines that spawn in either even or odd year – that is, the same species in the same river, but with a lack of genetic flow between populations. In vitro mixture of the two broodlines and later release of hybrids in the wild have shown that the second generation of hybrids had nearly 50% higher mortality rates (i.e., failure to return to spawn following release) when born from crossings of parents from different broodlines than when broodlines were not mixed (4).

CB_OutbreedingDepression Figure2
Survival rates of different genetic lineages of largemough bass following inoculation of a pathogen (3). The experiment was done in 2002 with 144 fish, each aged 13-14 months and bred from parents captured in 1995 in the basins of the Mississippi River and the Great Lakes. Parents resulted from crossings of adults from the same basin (blue and green lines), and 1st- and 2nd-generation hybrids were from crossings of parents from different basins. Viruses were inoculated 7 days (grey dashed line) after individuals had acclimated in each of 12 experimental aquaria (12 fish per aquarium). Graphs show the cumulative percentage of survivors on each day within 3 weeks following inoculation. By the end of the experiment, survival in the 2nd generation of infected hybrids (< 40%) was half that of the 1st generation of infected hybrids and their infected parents (> 80 %). All control parents (not infected) survived, so observed mortality in infected lineages was not caused by manipulation.

To intervene or not to intervene, that is the question

In translocations, the opposite of outbreeding depression is ‘hybrid vigour’ (also known as ‘heterosis’), that is, when foreign individuals enhance fertility and/or survival rates of native populations, and can in fact prompt population recovery from depletion (‘genetic rescue’; 5). An emblematic instance is that of the Florida panther (Puma concolor coryi). Hunting over the 20th Century reduced the subspecies to ~ 40 individuals, showing obvious signs of inbreeding depression (e.g., malformation of testicles, heart, tail and semen). In 1995, the supplementation of 8 females from the closest population of the species (Texas) has boosted the population up to some 100 individuals currently, yet at the expense of a 20% loss in genetic diversity (6). But because inbreeding and outbreeding depression are caused by different mechanisms, populations can have both (e.g., 7, 8). As a result, translocations might elicit outbreeding depression, regardless of whether inbreeding depression is counteracted.Translocations are attractive conservation measures if the available budget allows – modern technology can indeed move around many individuals, be they daisies or rhinos. Such passive genetic manipulations have become a major tool in conservation biology and they are likely to become more and more popular in the future (9). However, given a threat and an endangered species, if risks such as incurring outbreeding depression exist, the wisest action might well be to do nothing but invest in protecting the habitat of the endangered populations.Preventing extinctions will always be more effective and cheaper than trying to restore depleted populations.

Salvador Herrando-Pérez

References

  1. Edmands, S. (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Molecular Ecology, 16: 463-475
  2. Frankham, R. et al. (2011) Predicting the Probability of Outbreeding Depression. Conservation Biology, 25: 465-475
  3. Goldberg, T. L. et al. (2005) Increased infectious disease susceptibility resulting from outbreeding depression. Conservation Biology, 19: 455-462
  4. Gharrett, A. J. et al. (1999) Outbreeding depression in hybrids between odd- and even-broodyear pink salmon. Aquaculture, 173: 117-129
  5. Tallmon, D. A. et al. (2004) The alluring simplicity and complex reality of genetic rescue. Trends in Ecology and Evolution, 19: 489-496
  6. Hedrick, P. W. & Fredrickson, R. (2010) Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conservation Genetics, 11: 615-626
  7. Fenster, C. B. & Galloway, L. F. (2000) Inbreeding and outbreeding depression in natural populations of Chamaecrista fasciculata (Fabaceae). Conservation Biology, 14: 1406-1412
  8. Marshall, T. C. & Spalton, J. A. (2000) Simultaneous inbreeding and outbreeding depression in reintroduced Arabian oryx. Animal Conservation, 3: 241-248
  9. Frankham, R. (2010) Challenges and opportunities of genetic approaches to biological conservation. Biological Conservation, 143: 1919-1927

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14 01 2013
marioquevedo

Great post; I’d bet I’m not the only one who thinks more often on the inbreeding part of the coin rather than balancing both sides.

I have a minor “but” though, not so much a critic as a personal sort of frustration: the finishing lines read “the wisest action might well be to do nothing but invest in protecting the habitat of the endangered populations”.

I’ve said that myself before to managers, but every time it feels just too vague. Surely much fuzzier than the reasoning often used to critically evaluate their management actions.

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